Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner

Traffic

Volumn 6, Issue 2, 2005, Pages 131-143

  Savina, Ariel ^a   Fader, Claudio M ^a   Damiani, María T ^a   Colombo, María Isabel ^a  

^a Instituto de Histologia y Embriologia   (Argentina)

Author keywords

Calcium; Exosomes; Monensin; Multivesicular body; Rab11

Indexed keywords

CALCIUM; CALCIUM CHELATING AGENT; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; RAB PROTEIN;

ARTICLE; CALCIUM CELL LEVEL; CELL FUNCTION; CELL FUSION; CELL MEMBRANE; CELL STRAIN K 562; CELL VACUOLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION;

CALCIUM; CELL LINE; CELL MEMBRANE; CHELATING AGENTS; CYTOSOL; EGTAZIC ACID; ENDOSOMES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HUMANS; IONOPHORES; K562 CELLS; KINETICS; MACROPHAGES; MEMBRANE FUSION; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MONENSIN; MUTATION; RAB GTP-BINDING PROTEINS; TRANSPORT VESICLES; XANTHENES;

EID: 12744269555     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2004.00257.x     Document Type: Article

References (60)

1. Piper RC, Luzio JP. Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2001;2:612-621.
2. Gruenberg J, Stenmark H. The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 2004;5:317-323.
3. Harding C, Levy MA, Stahl P. Morphological analysis of ligand uptake and processing the role of multivesicular endosomes and CURL in receptor-ligand processing. Eur J Cell Biol 1985;36:230-238.
4. Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 1985;101:942-948.
5. Futter CE, Pearse A, Hewlett LJ, Hopkins CR. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 1996;132:1011-1023.
6. Felder S, Miller K, Moehren G, Ullrich A, Schlessinger J, Hopkins CR. Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 1990;61:623-634.
7. Bache KG, Raiborg C, Mehlum A, Stenmark H. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J Biol Chem 2003;278:12513-12521.
8. Raiborg C, Bache KG, Mehlum A, Stang E, Stenmark H. Hrs recruits clathrin to early endosomes. EMBO J 2001;20:5008-5021.
9. Raiborg C, Stenmark H. Hrs and endocytic sorting of ubiquitinated membrane proteins. Cell Struct Funct 2002;27:403-408.
10. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD. Escrt III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 2002;3:271-282.
11. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 2002;3:283-289.
12. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 2001; 106: 145-155.
13. Bishop NE. Dynamics of endosomal sorting. Int Rev Cytol 2003;232: 1-57.
14. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multi-vesicular bodies and alpha-granules. Blood 1999;94:3791-3799.
15. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-1172.
16. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998;4:594-600.
17. Johnstone RM, Adam M, Pan BT. The fate of the transferrin receptor during maturation of sheep reticulocytes in vitro. Can J Biochem Cell Biol 1984;62:1246-1254.
18. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 1983;33:967-978.
19. Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 2000;165:1259-1265.
20. de Gassart A, Geminard C, Fevrier B, Raposo G, Vidal M. Lipid raft-associated protein sorting in exosomes. Blood 2003;102:4336-4344.
21. Gerber SH, Sudhof TC. Molecular determinants of regulated exocytosis. Diabetes 2002;51(Suppl. 1):S3-S11.
22. Savina A, Furlan M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 2003;278:20083-20090.
23. Pfeffer SR. Rab GTPases: master regulators of membrane trafficking. Curr Opin Cell Biol 1994;6:522-526.
24. Brennwald P. Reversal of fortune. Do Rab GTPases act on the target membrane? J Cell Biol 2000;149:1-4.
25. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
26. Green EG, Ramm E, Riley NM, Spiro DJ, Goldenring JR, Wessling-Resnick M. Rab11 is associated with transferrin-containing recycling compartments in K562 cells. Biochem Biophys Res Commun 1997;239:612-616.
27. Chen W, Feng Y, Chen D, Wandinger-Ness A. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 1998;9: 3241-3257.
28. Urbe S, Huber LA, Zerial M, Tooze SA, Parton RG. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett 1993;334:175-182.
29. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996;135:913-924.
30. Savina A, Vidal M, Colombo MI. The exosome pathway in K562 cells is regulated by Rab11. J Cell Sci 2002;115:2505-2515.
31. 2+ exchange and its implications for calcium homeostasis in primary cultured rat brain microvascular endothelial cells. J Physiol 1999;515(Pt 1):147-155.
32. Vidal M, Mangeat P, Hoekstra D. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J Cell Sci 1997;110 (16):1867-1877.
33. Stein BS, Bensch KG, Sussman HH. Complete inhibition of transferrin recycling by monensin in K562 cells. J Biol Chem 1984;259:14762-14772.
34. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 1998;392:193-197.
35. Matsuo H, Chevallier J, Mayran N, Le BI, Ferguson C, Faure J, Blanc NS, Matile S, Dubochet J, Sadoul R, Parton RG, Vilbois F, Gruenberg J. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 2004;303:531-534.
36. + T cells by dendritic cell-derived exosomes. Nat Immunol 2002;3:1156-1162.
37. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 2003;278:10963-10972.
38. Mobius W, van Donselaar E, Ohno-Iwashita Y, Shimada Y, Heijnen HF, Slot JW, Geuze HJ. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 2003;4:222-231.
39. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;262:9412-9420.
40. Johnstone RM. Cleavage of the transferrin receptor by human granulocytes: differential proteolysis of the exosome-bound TFR. J Cell Physiol 1996;168:333-345.
41. Geminard C, Nault F, Johnstone RM, Vidal M. Characteristics of the interaction between Hsc70 and the transferrin receptor in exosomes released during reticulocyte maturation. J Biol Chem 2001;276, 9910-9916.
42. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983;97:329-339.
43. Ren M, Xu G, Zeng J, Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci U S A 1998;95:6187-6192.
44. Roberts RL, Barbieri MA, Pryse KM, Chua M, Morisaki JH, Stahl PD. Endosome fusion in living cells overexpressing GFP-rab5. J Cell Sci 1999;112:3667-3675.
45. Diaz R, Mayorga LS, Mayorga LE, Stahl P. In vitro clustering and multiple fusion among macrophage endosomes. J Biol Chem 1989;264:13171-13180.
46. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 1997;139:639-649.
47. Jahn R, Lang T, Sudhof TC. Membrane fusion. Cell 2003;112:519-533.
48. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 2000;28: 537-545.
49. 2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 1998;396:575-580.
50. Holroyd C, Kistner U, Annaert W, Jahn R. Fusion of endosomes involved in synaptic vesicle recycling. Mol Biol Cell 1999;10: 3035-3044.
51. Mills IG, Urbe S, Clague MJ. Relationships between EEA1 binding partners and their role in endosome fusion. J Cell Sci 2001;114: 1959-1965.
52. Gruenberg J, Howell KE. Membrane traffic in endocytosis: insights from cell-free assays. Annu Rev Cell Biol 1989;5:453-481.
53. Mullock BM, Bright NA, Fearon CW, Gray SR, Luzio JP. Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J Cell Biol 1998;140:591-601.
54. Rieu S, Geminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin α4β1. Eur J Biochem 2000;267:583-590.
55. Vidal MJ, Stahl PD. The small GTP-binding proteins Rab4 and ARF are associated with released exosomes during reticulocyte maturation. Eur J Cell Biol 1993;60:261-267.
56. 2+-regulated versus constitutive exocytosis. J Neurosci 2003;23:10531-10539.
57. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood 1989;74:1844-1851.
58. Ho IK, Ellman GL. Triton solubilized acetylcholinesterase of brain. J Neurochem 1969;16:1505-1513.
59. Willem J, ter Beest M, Scherphof G, Hoekstra D. A non-exchangeable fluorescent phospholipid analog as a membrane traffic marker of the endocytic pathway. Eur J Cell Biol 1990;53:173-184.
60. Geminard C, de Gassart A, Blanc L, Vidal M. Degradation of AP2 during reticulocyte maturation enhances binding of Hsc70 and Alix to a common site on TfR for sorting into exosomes. Traffic 2004: 5:183-185.